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Bosniak Category IIF and III


Cystic Renal Lesions: Outcomes
and Associations1
ORIGINAL RESEARCH

Andrew D. Smith, MD
Purpose: To evaluate clinical outcomes, pathologic subtypes, met-
Erick M. Remer, MD
astatic disease rate, and clinical features associated with
Kelly L. Cox, MD
malignancy in Bosniak category IIF and III cystic renal
Michael L. Lieber, MS lesions.
Brian C. Allen, MD2
Shetal N. Shah, MD Materials and This retrospective study was institutional review board
Brian R. Herts, MD Methods: approved and HIPAA compliant. Informed consent was
waived. Radiology and hospital information systems were
searched for Bosniak IIF and Bosniak III lesions in com-
puted tomographic (CT) reports from January 1, 1994 to
August 31, 2009. Patients 18 years and older with unen-
hanced and contrast material–enhanced CT results and
with lesions either surgically resected or with 1 year or
more of surveillance were included. Data recorded were
history of renal cell carcinoma, number of renal lesions,
presence of a coexistent solid renal mass, surgical patho-
logic findings, and presence of metastatic disease from a
renal malignancy. Sixty-two patients with 69 Bosniak IIF
lesions and 131 patients with 144 Bosniak III lesions were
identified. Proportions from independent groups were com-
pared by using the Fisher exact test; continuous variables
were compared by using a two-tailed two-sample t test or
a Wilcoxon two-sample test.

Results: The malignancy rate of resected Bosniak IIF lesions was


25% (four of 16) and that for Bosniak III lesions was 54%
(58 of 107) (P = .03). Thirteen percent (nine of 69) of Bos-
niak IIF lesions progressed at follow-up, and 50% (four of
eight) of these resected cysts were malignant. History of
primary renal malignancy, coexisting Bosniak category IV
lesion and/or solid renal mass, and multiplicity of Bosniak
III lesions were each associated with an increased malig-
nancy rate in Bosniak III lesions. No patients developed
locally advanced or metastatic disease from a Bosniak IIF
1
or III lesion.
From the Section of Abdominal Imaging, Imaging
Institute (A.D.S., E.M.R., K.L.C., M.L.L., B.C.A., S.N.S.,
B.R.H.), Glickman Urological and Kidney Institute (E.M.R., Conclusion: Although the malignancy rate in surgically excised Bosniak
B.R.H.), and Department of Quantitative Health Sciences IIF and Bosniak III cystic renal lesions was 25% and 54%,
(M.L.L.), Cleveland Clinic Foundation, 9500 Euclid Ave, respectively, in our study, the malignancy rate was higher
A21, Cleveland, OH, 44195; Department of Radiology, in patients with a history of primary renal malignancy or
University of Mississippi Medical Center, Jackson, Miss coexisting Bosniak IV lesion and/or solid renal neoplasm.
(A.D.S.). Received May 5, 2011; revision requested June
14; revision received August 5; accepted August 10; final
version accepted August 23. Address correspondence to
q
RSNA, 2011
E.M.R. (e-mail: remere1@ccf.org).
2
Current address: Section of Abdominal Imaging, De-
partment of Radiology, Wake Forest University Baptist
Medical Center, Winston-Salem, NC.

q
RSNA, 2011

152 radiology.rsna.org n Radiology: Volume 262: Number 1—January 2012


GENITOURINARY IMAGING: Bosniak Category IIF and III Lesions Smith et al

T
he Bosniak renal cyst classification complex than Bosniak II lesions but not or Bosniak III lesions in which biopsy
system, first described in 1986 (1), complex enough to be characterized as and ablation were percutaneously per-
is a well-established, widely used Bosniak III lesions. Bosniak category formed and those lesions that were
method that uses computed tomographic IIF cystic renal lesions generally un- not resected but had less than 1 year
(CT) findings to categorize cystic renal dergo imaging surveillance to demon- of imaging follow-up were excluded from
masses into groups on the basis of im- strate stability over the course of time, analysis. Patients with von Hippel-Lindau
aging features associated with malig- a feature associated with benignity (9). syndrome were excluded from analysis
nancy. In brief, Bosniak category I and There have been several studies evalu- because the great majority of cystic re-
Bosniak category II cystic renal lesions ating surveillance of Bosniak IIF lesions nal neoplasms in these patients are ma-
are simple and mildly complex cysts, re- (7,9), but because they are believed to lignant clear cell renal cell carcinoma
spectively, and require no further eval- be benign, there are few studies that (RCC).
uation. Bosniak category IV cystic renal have evaluated resected Bosniak IIF le- A total of 308 patients with Bosniak
lesions are almost certainly malignant sions (10). IIF and/or Bosniak III lesions were iden-
and are resected in clinically able pa- We performed a retrospective re- tified. Of these, 113 patients were ex-
tients. Bosniak category III cystic renal view of Bosniak IIF and Bosniak III le- cluded from analysis because of lack of
lesions are indeterminate in malignant sions to evaluate the clinical outcomes, surgical excision with less than 1 year
potential and most commonly managed pathologic diagnoses, metastatic disease of imaging follow-up. Seven of these pa-
with surgical excision. While the malig- rate, and clinical features associated tients with eight Bosniak III lesions had
nancy risk of Bosniak III cystic lesions is with malignancy. benign pathologic findings at percutane-
thought to be approximately 50% (2), ous biopsy (seven core-needle biopsies
reported malignancy rates range from and one fine-needle aspiration biopsy)
31% (3) to 100% (4). Furthermore, stud- Materials and Methods and were excluded because of potential
ies published to date have included rel- sampling error. An additional two pa-
atively small numbers of lesions: Four Identification of Patients with Bosniak IIF tients were excluded because of unclear
studies described fewer than 15 Bosniak and III Cystic Renal Lesions surgical pathologic findings (n = 1) or a
III lesions each (3–6), one included 33 Informed consent was waived in this history of von Hippel-Lindau syndrome
(7), and the largest included 49 (8). Bos- institutional review board–approved, (n = 1). A total of 69 Bosniak IIF le-
niak category IIF is a modification of the Health Insurance Portability and Ac- sions in 62 patients and 144 Bosniak III
initial classification used to describe a countability Act–compliant retrospective lesions in 131 patients were included in
group of cystic lesions that are more study. A database with integrated data the final analysis.
from our radiology (Syngo Workflow; A CT study both without contrast
Advances in Knowledge Siemens Medical USA, Malvern, Pa) material and with intravenous contrast
n Fifty-four percent (58 of 107) of and hospital (Epic Systems, Verona, Wis) material was used for initial classifica-
resected Bosniak category III information systems was searched for tion with the Bosniak grading system
cystic renal lesions and 25% the term “Bosniak” combined with “IIF” in 92% (178 of 193) of patients, and
(four of 16) of Bosniak category or “2F” or “III” or “3” from January 1, MR imaging without and with intrave-
IIF lesions were malignant, but 1994 to August 31, 2009 in reports nous contrast material was used in 8%
resected Bosniak IIF lesions were from CT or magnetic resonance (MR)
highly selected and had a high imaging studies performed in patients
18 years or older. The search of approx- Published online before print
number of risk factors associated 10.1148/radiol.11110888 Content code:
with malignancy. imately 100 000 reports yielded 3215
examinations. Inclusion criteria for the Radiology 2012; 262:152–160
n A history of primary renal malig- study group were unenhanced and con-
nancy, coexisting Bosniak cate- trast material–enhanced CT examination
Abbreviation:
gory IV cystic renal lesion and/or RCC = renal cell carcinoma
results and surgical resection of the lesion
solid renal mass (common in or 1 year or more of imaging follow-up Author contributions:
patients with resected Bosniak of the lesion. Patients with Bosniak IIF Guarantors of integrity of entire study, A.D.S., E.M.R.;
IIF cystic renal lesions), and mul- study concepts/study design or data acquisition or data
tiplicity of Bosniak III cystic renal analysis/interpretation, all authors; manuscript drafting
lesions were all associated with Implication for Patient Care or manuscript revision for important intellectual content,
all authors; manuscript final version approval, all au-
an increased risk of malignancy. n These data support current rec- thors; literature research, A.D.S., E.M.R., K.L.C., S.N.S.,
n No Bosniak IIF or III cystic renal ommendations for observation in B.R.H.; clinical studies, A.D.S., E.M.R., S.N.S.; statistical
lesion progressed to a Bosniak IV patients with Bosniak IIF or III analysis, A.D.S., K.L.C., M.L.L.; and manuscript editing,
lesion or solid renal neoplasm, cystic renal lesions and multiple all authors
and no patient developed locally comorbidities or short life Potential conflicts of interest are listed at the end
advanced or metastatic disease. expectancy. of this article.

Radiology: Volume 262: Number 1—January 2012 n radiology.rsna.org 153


GENITOURINARY IMAGING: Bosniak Category IIF and III Lesions Smith et al

(15 of 193) of patients for the initial determine if multiplanar reformations Statistical Analysis
classification. If MR imaging was the were obtained and archived. For patients The homogeneity hypothesis for pro-
first examination performed, CT per- with surgical resection of Bosniak IIF portions from independent groups was
formed later in the patient’s clinical and/or Bosniak III lesions, the date of assessed by using the Fisher exact test.
course was utilized for lesion character- surgery was recorded, and the interval Continuous variables were compared
ization in this study. from initial Bosniak classification to by using a two-tailed two-sample t test
surgery was calculated. The pathology or Wilcoxon two-sample test. A statis-
Data Collection and Surgical Pathologic specimen reports from these patients tically significant difference was consid-
Correlation and Follow-up were reviewed, and the lesions were ered to be indicated by a P value less
Clinical data recorded from the elec- classified as benign or malignant. The than .05.
tronic medical record included patient Fuhrman nuclear grade of malignant le-
sex; date of birth; age at initial appli- sions was recorded. For those patients
cation of Bosniak classification; date of without surgical treatment, the date of Results
initial imaging examination used for initial Bosniak classification of the cys- Nearly all of the imaging studies (191
Bosniak classification; specialty of the tic renal lesion(s) and the date of the [99%] of 193) were interpreted by
physician who ordered the imaging study last CT imaging study and last clinical fellowship-trained abdominal radiolo-
used to classify the lesion (urologist note to calculate duration of imaging gists; only two studies were interpreted
or nonurologist); history of hemodi- surveillance and duration of clinical sur- by general practice community radiolo-
alysis; history of malignancy (primary veillance, respectively, were used. The gists. The section thickness of axial CT
renal tumor or neoplasm originating in frequency of reclassification of Bosniak images (170 of 178 CT examinations
another organ) or Bosniak IV lesion; IIF lesions to Bosniak III lesions as re- available for review) was 3 mm in 81%
date of the last clinical note; and, when ported by the interpreting radiologist (137 of 170) of cases and 5 mm in 19%
present, the date of development of met- was noted. The application of Bosniak (33 of 170) of cases. Most of the CT
astatic disease from a primary renal classification by the initial interpreting studies (158 [82%] of 193) had mul-
malignancy. The imaging reports from radiologist was not reevaluated. tiplanar reformations available to the
the time of initial application of the interpreting radiologist at the time of
Bosniak criteria until the last available Imaging Technique diagnosis.
imaging report were assessed for each CT imaging at our institution was ob- Characteristics and treatment of pa-
patient, and the date of any reclassifica- tained with multidetector CT scanners tients with Bosniak IIF and Bosniak III
tion of a Bosniak category was recorded. (Emotion Duo, Volume Zoom, Sensation lesions are shown in Table 1. Seventy-
All Bosniak IIF lesions that were later 16, or Sensation 64; Siemens Medical, seven percent (101 of 131) of patients
categorized as Bosniak III lesions were Forchheim, Germany). Only patients who with Bosniak III lesions underwent sur-
categorized as Bosniak III lesions in the underwent CT imaging without contrast gical excision of the lesion(s) rather
pathologic and clinical analysis. Because material and CT imaging with intrave- than imaging surveillance. In contrast,
a number of Bosniak IIF and III lesions nous contrast material were included; 21% (13 of 62) of patients with Bosniak
were reclassified at follow-up imaging, our standard renal CT protocol included IIF lesions underwent surgical excision.
a radiologist with 17 years of experience unenhanced imaging of the kidneys, fol- Sixteen Bosniak IIF lesions in 13 pa-
(E.M.R.) reevaluated the images to de- lowed by a 20-mL test bolus of contrast tients were resected, and six patients
termine whether reclassification resulted material, usually iopromide (300 mg of had a coexisting Bosniak IV lesion and/
from a change in the lesion imaging iodine per milliliter, Ultravist 300; Bayer or solid renal mass (five ipsilateral and
characteristics or, if no change, from Healthcare, Berlin, Germany), for arte- one contralateral to the Bosniak IIF le-
differing opinions of the original inter- rial enhancement timing. Postcontrast sions), three patients had a history of
preting radiologists. imaging was performed 5 seconds after primary renal malignancy, two patients
In addition, the practice type of the the optimal arterial time (vascular and had an ipsilateral Bosniak III lesion,
radiologist who initially classified the corticomedullary phase) and then again three patients requested definitive sur-
lesion (fellowship-trained academic or 2 minutes after the start of contrast ma- gical treatment, and two patients had
community-based radiologist), the number terial injection (nephrographic phase). recurrent cysts after aspiration and sus-
and side (right and/or left kidney) of the The specific CT parameters, contrast ma- picion for malignancy by the urologist.
Bosniak IIF or III lesions, the number terial injection rate, and contrast ma- Patients with Bosniak IIF lesions were
and side of coexisting Bosniak IV le- terial dose were not consistent in this significantly more likely to undergo re-
sions and/or solid renal mass, and the retrospective study. Almost all CT exam- section rather than imaging surveillance
type of imaging studies used to initially inations were performed with scanners when there was a coexisting Bosniak
classify the Bosniak cystic lesions were with at least four detector rows. Eight IV lesion and/or solid renal neoplasm
recorded. studies were performed prior to 1999 (P = .0001).
All imaging studies were reviewed to for which scanner type could not be Nine cystic renal lesions, in eight pa-
identify the axial section thickness and to determined. tients, initially classified as Bosniak IIF

154 radiology.rsna.org n Radiology: Volume 262: Number 1—January 2012


GENITOURINARY IMAGING: Bosniak Category IIF and III Lesions Smith et al

Table 1
Characteristics and Treatment of Patients with Bosniak IIF and III Lesions
Bosniak IIF Lesions Bosniak III Lesions
Parameter Surgical Excision Imaging Surveillance P Value Surgical Excision Imaging Surveillance P Value

No. of patients 13 49 … 101 30 …


No. of Bosniak IIF or III lesions 16 53 … 107 37 …
Median age (y)* 52 (33–74) 66 (37–87) .0043† 57 (27–80) 68 (43–89) .00007†
Percentage of imaging studies ordered by a 100 (13/13) 57 (28/49) .0026‡ 90 (91/101) 63 (19/30) .0012‡
urologist
Percentage of patients with history of 0 (0/13) 20 (10/49) .10 3 (3/101) 27 (8/30) .0003‡
nonrenal metastatic neoplasm
Percentage of patients with coexisting Bosniak 46 (6/13) 0 (0/49) .0001‡ 16 (16/101) 23 (7/30) .41
IV lesion and/or solid renal mass
Percentage of patients with history of 23 (3/13) 4 (2/49) .06§ 7 (7/101) 30 (9/30) .0021‡
malignant primary renal neoplasm
Median duration of imaging surveillance after … 2.4 (1.0–8.0) … … 3.8 (1.0–8.2) …
classification (y)*
Median duration of clinical surveillance after 3.1 (0.1–7.4) 3.6 (1.0–8.5) … 2.1 (0–11.1) 4.4 (1.0–15.2) …
classification (y)*
Percentage of patients with metastatic disease 0 (0/13) 0 (0/49) … 0 (0/101) 0 (0/30) …
from a primary renal malignancy

* Data in parentheses are ranges.



Statistically significant P value (,.05, two-sample t test).

Statistically significant P value (,.05, Fisher exact test).
§
Marginally statistically significant P value (.05 , P , .10, Fisher exact test).

lesions (nine [13%] of 69) were later years). Patients with either Bosniak IIF nuclear grade was available for 57 of
reclassified as Bosniak III lesions at a or Bosniak III lesions who underwent the 58 resected malignant Bosniak III
median time of 0.5 years (range, 0.2– imaging surveillance were on average lesions and was grade 1 in 19% (11 of
2.0 years) after the initial classification significantly older than those patients 57), grade 2 in 61% (35 of 57), grade 3
as a Bosniak IIF lesion (Fig 1). A single who underwent surgical excision, with a in 19% (11 of 57), and grade 4 in 0% (0
radiologist (E.M.R.) reviewed these pa- mean difference in both cases of greater of 57) of lesions. Clear cell carcinoma
tients’ studies and determined that mor- than 10 years (Table 1). Clinical history was the most prevalent malignant neo-
phologic changes led to reclassification that may have affected the decision to plasm (28 [48%] of 58), and the major-
of three lesions (Fig 2), Bosniak III was perform surgical resection such as co- ity of benign lesions (26 [53%] of 49)
the appropriate original classification existing renal lesions, history of nonre- were epithelial or fibrous cysts.
in four lesions (Fig 3), and Bosniak IIF nal malignancy, and ordering physician The association of three factors and
was the appropriate classification in two are listed in Table 1. the prevalence of malignancy in Bosniak
lesions such that the lesion should not The malignancy rate of and specific IIF and Bosniak III lesions were evalu-
have been reclassified. Eight of these le- pathologic subtypes of resected Bosniak ated: coexisting Bosniak III lesion, co-
sions were resected with a malignancy IIF and Bosniak III lesions are shown in existing Bosniak IV lesion and/or solid
rate of 50% (four of eight). One patient Table 2. Fifty-four percent (58 of 107) mass, and a history of malignant renal
had a history of contralateral partial of resected Bosniak III lesions were neoplasm (Table 3). Two patients had
nephrectomy for papillary RCC, was malignant and 25% (four of 16) of re- both Bosniak IIF and Bosniak III lesions.
treated with periodic surveillance imag- sected Bosniak IIF lesions were malig- The first patient had ipsilateral solitary
ing for 1.9 years, and subsequently was nant, which was a significant difference Bosniak IIF and Bosniak III lesions with
lost to follow-up. (P = .03, Fisher exact test; estimated a benign cortical cyst and cystic nephro-
After initial CT categorization, pa- odds ratio = 3.55; 95% confidence in- ma, respectively, at surgical pathologic
tients with Bosniak IIF lesions under- terval: 1.08, 11.72). The Fuhrman nu- findings. The second had ipsilateral
went surgery at a median of 0.1 year clear grade was only available for three solitary Bosniak IIF and Bosniak III
(range, 0–6.1 years), and those with of four resected malignant Bosniak IIF lesions and two contralateral Bosniak
Bosniak III lesions underwent surgery lesions and was grade 1 for one lesion IIF lesions that were all benign cortical
at a median of 0.1 year (range, 0–2.1 and grade 2 for two lesions. Fuhrman cysts according to surgical pathologic

Radiology: Volume 262: Number 1—January 2012 n radiology.rsna.org 155


GENITOURINARY IMAGING: Bosniak Category IIF and III Lesions Smith et al

Figure 1 a coexisting Bosniak IV lesion at the


time of Bosniak classification.
The duration of imaging and clinical
surveillance of Bosniak IIF and Bosniak
III lesions included in the study is pre-
sented in Table 1. The majority of pa-
tients with resected Bosniak IIF (nine
[69%] of 13) and Bosniak III lesions
(88 [87%] of 101) had no imaging fol-
low-up after surgery. Despite a higher
percentage of patients with a coexist-
ing Bosniak IV lesion and/or solid renal
neoplasm or history of malignant pri-
mary renal neoplasm in patients with
Bosniak III lesions being treated with
imaging surveillance of 1 year or longer
compared with surgical excision, no
patient in this study developed locally
advanced or metastatic disease from
a cystic renal neoplasm. No Bosniak
III lesions (n = 144) progressed to a
Bosniak IV lesion; seven were down-
graded to Bosniak IIF lesions. Median
imaging follow-up was 3.8 years (range,
1.0–8.2 years), and median clinical
follow-up was 4.4 years (range, 1.0–
15.2 years) for patients with Bosniak
III lesions managed by using imaging
surveillance (Table 1).

Discussion
The Bosniak classification system is
Figure 1: Transverse baseline (a) unenhanced and (b) nephrographic phase CT images in 69-year-old widely acknowledged as a useful guide-
man with a cystic renal lesion show thick partially calcified wall (arrow) with perceived enhancement inter- line for managing cystic renal masses
preted as Bosniak IIF lesion. Transverse (c) unenhanced and (d) nephrographic phase CT images at 6-month (11). The malignancy rate of 54% (58
follow-up show interval development of ill-defined enhancement along the posterior wall (arrow) leading to of 107) in our patient population is
reclassification as Bosniak III lesion. Pathologic diagnosis was benign cyst with fibrous wall. consistent with the previously published
and widely held belief that approxi-
findings. For Bosniak IIF lesions, sig- patients with benign Bosniak IIF lesions mately 50% of Bosniak III lesions are
nificantly more lesions were malignant (n = 9), the median age was 48 years malignant. While previous studies have
when the patient had a coexisting (range, 33–74 years) (P = .13, Wilcoxon shown a surprising variability in the
Bosniak IV lesion and/or a solid mass. two-sample test). The median age of pa- percentage of malignant Bosniak III
For Bosniak III lesions, any of the three tients with malignant Bosniak III lesions cysts (31%–100%), these numbers were
factors was associated with a signifi- (n = 55) was 58 years (range, 27–80 based on small series that used older
cantly higher percentage of malignant years), and for patients with benign CT technology. A weighted average from
lesions. Two of these factors were more Bosniak III lesions (n = 46), the median six studies that each included more
common in patients with Bosniak III le- age was 57 years (range, 33–78 years) than 30 renal cystic masses found 65%
sions treated with imaging surveillance (P = .38, Wilcoxon two-sample t test). of Bosniak III lesions to be malignant
than resection (Table 1). A history of hemodialysis was un- (12). As far as we are aware, this series
Patient age was not significantly dif- common in our patient population. One of 107 resected Bosniak III lesions
ferent between patients with Bosniak patient with a single resected benign represents the largest report of path-
IIF and those with Bosniak III lesions. Bosniak III lesion was receiving hemo- ologically examined Bosniak III lesions
The median age of patients with ma- dialysis, and one patient with two re- imaged by using multiphasic multide-
lignant Bosniak IIF lesions (n = 4) was sected malignant Bosniak IIF lesions tector CT and multiphasic MR imaging
62 years (range, 50–71 years), and for was receiving hemodialysis but also had examinations.

156 radiology.rsna.org n Radiology: Volume 262: Number 1—January 2012


GENITOURINARY IMAGING: Bosniak Category IIF and III Lesions Smith et al

Figure 2 were classified by using the Bosniak


system. Thirteen percent of Bosniak IIF
lesions were reclassified as Bosniak III
lesions at surveillance imaging in our
series, which is similar to the 14.8% rate
in the O’Malley et al series ( 7 ), but
more than the 4.8% in 48 cysts in the
Israel and Bosniak series (9). Fifty per-
cent of those that were resected were
malignant. On the basis of image review,
reclassification in the series was more
commonly because of reader disagree-
ment than a morphologic change in the
lesion.
There was a surprisingly high ma-
lignancy rate of 25% (four of 16) in re-
sected Bosniak IIF lesions. However, the
number of resected Bosniak IIF lesions
was small and only reflected a subset of
Bosniak IIF lesions in the population.
The patient population with resected
Bosniak IIF lesions was highly selected
and had a higher number of risk fac-
tors associated with malignancy than
the imaging surveillance group. In our
series, in patients with a Bosniak IIF le-
sion and a coexistent Bosniak IV lesion
and/or solid mass, 71% (five of seven)
of the Bosniak IIF lesions were malig-
nant. Similarly, 67% (two of three) of
Bosniak IIF lesions in patients with a
history of RCC were malignant. These
correlations certainly suggest that there
Figure 2: Transverse baseline (a) unenhanced and (b) nephrographic phase CT images in 61-year-old are unaccounted for variables that could
woman with a cystic renal lesion show a multicystic lesion with multiple septa of varying thickness (arrow), have affected the malignancy rate in
and lesion was interpreted as Bosniak IIF. Transverse (c) unenhanced and (d) nephrographic phase CT resected Bosniak IIF lesions in this
images at 15-month follow-up show progressive septal thickening (arrow) that was categorized as Bosniak series.
III. Pathologic diagnosis was clear cell carcinoma. Bosniak IIF and Bosniak III lesions
encompassed a wide variety of neo-
The malignancy rate of 54% in our Bosniak criteria were developed at the plasms. While the most common malig-
series differs from the malignancy rate institution of O’Malley et al, the IIF nant renal tumor in the series was clear
of 82% in 33 resected Bosniak III cysts category was more likely to have been cell carcinoma, it represented less than
found by O’Malley et al (7). The high immediately adopted, universally used, 50% of the malignant cystic lesions. A
malignancy rate was attributed to the and understood. Furthermore, images cystic growth pattern is seen in only
addition of the Bosniak IIF category be- in the O’Malley series were read by 4%–15% of all RCCs (13) and occurs
tween the publication of older studies one of several faculty radiologists. This by four mechanisms: intrinsic unilocu-
and the analysis. The use of the Bosniak suggests that a small group may have lar cystic growth, intrinsic multilocular
IIF category was thought to increase evaluated these studies, leading to less cystic growth, origin in the epithelium
the accuracy of the classification system observer variability. Our images were of a simple cyst, or cystic necrosis (14).
by downgrading lesions that were not interpreted by a group of 12 fellowship- True cystic growth, rather than necro-
complex enough to be characterized as trained abdominal radiologists. While sis, appears to confer a better prognosis
category III but that were more complex they were all well acquainted with the (15). Several prior studies of cysts with
than category II lesions (9). There are Bosniak classification, it is unclear how Bosniak grading have concentrated on
several explanations why we may not often or consistently classifications were the distinction between malignant and
have found as high a malignancy rate applied because the search parameters benign lesions and have not reported
in our Bosniak III group. Because the for this study only captured lesions that the subtypes of carcinoma (3,6,8). The

Radiology: Volume 262: Number 1—January 2012 n radiology.rsna.org 157


GENITOURINARY IMAGING: Bosniak Category IIF and III Lesions Smith et al

Figure 3 if near water attenuation was measured


on precontrast CT images.
Clinical data and CT image findings
strongly affected the risk of malignancy
for complex cysts in this study. Seventy-
one percent (five of seven) of Bosniak
IIF lesions found in patients with a co-
existing Bosniak IV lesion and/or solid
renal mass were malignant, which oc-
curred significantly more often than if
either of these findings was not present.
The percentage of Bosniak III lesions
that were malignant was especially high
when associated with other Bosniak III
lesions in the same patient (10 [83%]
of 12), a coexisting Bosniak IV lesion
and/or solid renal mass (15 [83%] of
18), or a history of RCC (eight [100%]
of eight). This suggests that patient-
related factors that predispose to RCC
may be at work in these patients. As
with all Bosniak III cystic renal lesions,
surgery should be first-line management.
If there are contraindications to sur-
gery, imaging follow-up is a reasonable
approach.
None of the patients with Bosniak
IIF or Bosniak III lesions in this study
(n = 193) had progression to Bosniak
IV lesions or solid neoplasms, and none
developed locally advanced or meta-
static disease. If there is a continuous
spectrum such that some Bosniak III
Figure 3: Transverse baseline (a) unenhanced and (b) nephrographic phase CT images in 59-year-old lesions progress to Bosniak IV lesions,
woman with a cystic renal lesion show a thick wall (arrow in b), with linear and punctate calcifications the rate of progression was too low to
(arrows in a and c) that measured 30 HU on unenhanced images but did not enhance, and lesion was be captured in our series. Despite a
interpreted as Bosniak IIF. Transverse (c) unenhanced and (d) nephrographic phase CT images at 6-month higher number of potential risk factors
follow-up show no change, but the lesion was interpreted as Bosniak III, presumably because of measurable associated with malignant Bosniak III le-
wall enhancement (arrow in d). Pathologic diagnosis was benign cyst. sions in the imaging surveillance group
(n = 30), none of these consequences
presumption that a malignant cystic le- papillary RCC is hyperdense and ho- were detected with imaging follow-up
sion equates to a cystic clear cell car- mogeneously enhancing at CT (16). A for a median of 3.8 years (range, 1.0–
cinoma and that a benign cystic lesion papillary RCC can, however, occasion- 8.2 years) and clinical follow-up for a
equates to an epithelial cyst is false. In ally manifest as a cystic mass. This has median of 4.4 years (range, 1.0–15.2
truth, there are a host of benign and been attributed to inherent architecture years).
malignant cystic renal neoplasms, in- or secondary to cystic degeneration Although the rate of development of
cluding cystic clear cell carcinoma, mul- and extensive necrosis (17). One series metastatic disease found at short-term
tilocular cystic RCC, cystic nephroma, found that cystic degeneration was al- imaging surveillance for Bosniak IIF and
and mixed epithelial and stromal tumor most as likely to occur in papillary RCC Bosniak III lesions was 0% (0 of 193),
of the kidney. Each confers a different as in clear cell RCC (18). In addition, the long-term rate of development of
prognosis and potentially requires dif- some papillary RCC are known to en- metastatic disease remains unknown.
ferent therapy. hance only minimally after intravenous Despite a malignancy rate of more than
We were surprised to find that 25% contrast material administration. These 50% for Bosniak III lesions, there is no
(15 of 58) of malignant resected cys- minimally enhancing tumors may have prospective data to show that resection
tic lesions were papillary RCCs at his- been mistaken for cystic lesions at the improves survival. Given that nearly
topathologic examination. Typically, time of image interpretation, especially half of Bosniak III lesions are benign

158 radiology.rsna.org n Radiology: Volume 262: Number 1—January 2012


GENITOURINARY IMAGING: Bosniak Category IIF and III Lesions Smith et al

Table 2 vers evaluating the features that are used


Surgical Pathologic Findings in Excised Bosniak IIF and III Lesions to select a Bosniak category (20) and
agreement between category assign-
All Excised Bosniak IIF Lesions All Excised Bosniak III Lesions ments (6) have been previously eval-
Surgical Pathologic Finding (n = 16) (n = 107)
uated. A choice was made not to rein-
Malignant 25 (4/16)* 54 (58/107)* terpret studies by using expert readers,
Clear cell RCC 19 (3/16) 26 (28/107) with the hope that this series would
Papillary RCC … 14 (15/107) represent a real-world experience, not
Unclassified RCC … 5 (5/107) an idealized one. Third, we have no way
Mixed RCC 6 (1/16) 4 (4/107) of knowing how often or consistently
Multilocular cystic RCC … 5 (6/107) Bosniak criteria were applied to all cystic
Benign 75 (12/16) 46 (49/107) renal lesions encountered at CT imaging,
Benign epithelial or fibrous cyst 31 (5/16) 24 (26/107) because the search parameters for this
Cystic nephroma 25 (4/16) 12 (13/107) study only captured lesions that were
Mixed epithelial stromal tumor … 1 (1/107) classified by using the Bosniak system.
Oncocytoma … 1 (1/107) Fourth, for patients with resected
Other benign tissue or few atypical cells 19 (3/16) 8 (8/107)
Bosniak IIF lesions, the statistical power
Note.—Data are percentages, with numbers used to calculate percentages in parentheses. Percentages may not add up to associate malignant Bosniak IIF le-
because of rounding. sions with risk factors such as coexist-
* The malignancy rate of resected Bosniak IIF and III lesions was significantly different (P = .03, Fisher exact test). ing Bosniak III lesion or history of RCC
was limited by patient sample size, and
the lack of a significant P value does
not include or exclude an important
Table 3
clinical association (Table 3). Fifth, in
Risk Factors for Malignancy in Resected Bosniak IIF and III Lesions lesion-level analyses (Table 2), multiple
lesions within patients were treated
Prevalence of Malignant in Resected Prevalence of Malignant in Resected
Risk Factor Bosniak IIF Lesions (n = 16) Bosniak III Lesions (n = 107)
as statistically independent; therefore,
any intrapatient correlation due to clus-
Coexisting Bosniak III lesion tering was not accounted for in hypo-
Present 0 (0/2) 83 (10/12) thesis tests. We note that 23% (three
Absent 43 (6/14) 51 (48/95) of 13) of patients with surgically excised
P value .50 .036* Bosniak IIF lesions and 8% (eight of
Coexisting Bosniak IV lesion 101) of patients with surgically excised
and/or solid renal mass
Bosniak III lesions had more than one
Present 71 (5/7) 83 (15/18)
Bosniak IIF or Bosniak III lesion, and only
Absent 11 (1/9) 49 (44/89)
one patient had more than three. Last,
P value .035* .009*
the true malignancy rate of the Bosniak
History of malignant primary
IIF and Bosniak III lesions in patients
renal cell neoplasm
Present 67 (2/3) 100 (8/8)
who underwent imaging surveillance
Absent 31 (4/13) 45 (44/99) is not known, and the length of imag-
P value .52 .0067* ing follow-up may have been insuffi-
cient to detect imaging manifestations of
Note.—Unless otherwise indicated, data are percentages of patients, with numbers used to calculate percentages in malignancy.
parentheses.
In conclusion, 54% (58 of 107) of
* Significant P value (,.05) by using the Fisher exact test.
Bosniak III cystic renal lesions were ma-
lignant in our series, with clear cell car-
cinoma and papillary RCC most com-
and that the risk of metastatic disease case series; therefore, there was no mon. Thirteen percent (nine of 69) of
or local progression appears to be low, standardized follow-up interval and there Bosniak IIF lesions were reclassified at
our data support current recommenda- were changes in CT technology during follow-up and 50% (four of eight) of
tions for observation in patients with the time interval of the study. Second, these patients had malignant lesions.
Bosniak IIF or Bosniak III lesions and there were multiple readers who in- A history of primary renal malignancy,
multiple comorbidities or short life ex- terpreted the CT images that were in- coexisting Bosniak IV cystic renal lesion
pectancy (19). cluded in the study. Application of the and/or solid renal mass (common in
There were a number of limitations of Bosniak classification system is subjec- patients with resected Bosniak IIF cys-
our study. First, it was a retrospective tive, and the agreement between obser- tic renal lesions), and multiplicity of

Radiology: Volume 262: Number 1—January 2012 n radiology.rsna.org 159


GENITOURINARY IMAGING: Bosniak Category IIF and III Lesions Smith et al

Bosniak III cystic renal lesions were all evaluation of the usefulness of the Bosniak 13. Hartman DS, Davis CJ Jr, Johns T,
associated with an increased risk of classification system. Acad Radiol 1996; Goldman SM. Cystic renal cell carcinoma.
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tients with Bosniak IIF or III cystic renal Hartman DS, Christenson PJ. Cystic renal eds. Pathology and genetics of tumours of
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plasms, and none developed locally ad- 6. Siegel CL, McFarland EG, Brink JA, 15. Han KR, Janzen NK, McWhorter VC, et al.
vanced or metastatic disease. Fisher AJ, Humphrey P, Heiken JP. CT of Cystic renal cell carcinoma: biology and
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est: A.D.S. No potential conflicts of interest
tion. AJR Am J Roentgenol 1997;169(3):
to disclose. E.M.R. No potential conflicts of 16. Silverman SG, Mortele KJ, Tuncali K,
813–818.
interest to disclose. K.L.C. No potential con- Jinzaki M, Cibas ES. Hyperattenuating renal
flicts of interest to disclose. M.L.L. No po- 7. O’Malley RL, Godoy G, Hecht EM, masses: etiologies, pathogenesis, and imag-
tential conflicts of interest to disclose. B.C.A. ing evaluation. RadioGraphics 2007;27(4):
Stifelman MD, Taneja SS. Bosniak category
No potential conflicts of interest to disclose.
IIF designation and surgery for complex re- 1131–1143.
S.N.S. No potential conflicts of interest to
disclose. B.R.H. Financial activities related to nal cysts. J Urol 2009;182(3):1091–1095.
17. Vikram R, Ng CS, Tamboli P, et al. Papillary
the present article: none to disclose. Financial renal cell carcinoma: radiologic-pathologic
8. Curry NS, Cochran ST, Bissada NK. Cystic
activities not related to the present article: in-
renal masses: accurate Bosniak classification correlation and spectrum of disease. Radio-
stitution has grant from Siemens Medical for
requires adequate renal CT. AJR Am J Graphics 2009;29(3):741–754.
radiation dose research. Other relationships:
none to disclose. Roentgenol 2000;175(2):339–342.
18. Brinker DA, Amin MB, de Peralta-Venturina M,
9. Israel GM, Bosniak MA. Follow-up CT of Reuter V, Chan DY, Epstein JI. Exten-
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